Impact of Aneurysm Location on Cardiopulmonary Dysfunction after Subarachnoid Hemorrhage Nobutaka Horie, MD, PhD,* Eiji Isotani, MD, PhD,† Sumihisa Honda, PhD,‡ Hideyuki Oshige, MD, PhD,x and Izumi Nagata, MD, PhD,* on behalf of SAH PiCCO Study Group

Background: Cardiopulmonary dysfunction may occur after aneurysmal subarachnoid hemorrhage (SAH), but its characteristics have not been fully clarified. We investigated the impact of aneurysm location on systemic hemodynamics after SAH. Methods: This multicenter prospective cohort study measured hemodynamic parameters in relation to aneurysm location in patients with SAH using a singleindicator transpulmonary thermodilution system (PiCCO) on days 1-14. Results: Of 204 subjects enrolled, 58 had aneurysms of the anterior communicating artery (ACA), 61 of the middle cerebral artery (MCA), 57 of the internal carotid artery (ICA), and 28 of the vertebrobasilar artery (VA/BA). Patient characteristics were similar except for predominance of coiling in the VA/BA. Patients with ACA aneurysm had a lower systemic vascular resistance index (SVRI) in the acute phase and afterload mismatch (lower cardiac index [CI] and higher SVRI) in the spasm phase. Those with ICA aneurysm had a lower CI in the acute phase, and those with VA/BA aneurysm had a warm shock-like condition (higher CI and lower SVRI) in the spasm phase. Patients with MCA aneurysm showed no specific characteristics in CI and SVRI with a significant improvement in B-type natriuretic peptide. Extravascular lung water index was high independent of left cardiac dysfunction. In multivariate analysis, age and ACA were independently related to poor global ejection fraction after SAH. Conclusions: Aneurysm location affects cardiac output, vascular resistance, and pulmonary edema in biphasic fashion. Patient age and location of aneurysm in the ACA may be risk factors for cardiac failure after SAH. Key Words: Subarachnoid hemorrhage—aneurysm location—systemic hemodynamics— cardiopulmonary dysfunction. Ó 2014 by National Stroke Association

From the *Department of Neurosurgery, Nagasaki University School of Medicine, Nagasaki; †Emergency and Critical Care Center, Tokyo Women’s Medical University Medical Center East, Tokyo; ‡Graduate School of Biomedical Sciences, Nagasaki University, Nagasaki; and xDepartment of Neurosurgery, Kansai Medical University, Osaka, Japan. Received January 21, 2014; revision received March 20, 2014; accepted April 18, 2014. Clinical Trial Registration: http://apps.who.int/trialsearch/trial. aspx?trialid5JPRN-UMIN000003794. Address correspondence to Nobutaka Horie, MD, PhD, Department of Neurosurgery, Nagasaki University School of Medicine, 17-1 Sakamoto, Nagasaki 852-8501, Japan. E-mail: nobstanford@ gmail.com. 1052-3057/$ - see front matter Ó 2014 by National Stroke Association http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2014.04.030

Cerebral vasospasm is a leading cause of morbidity and mortality in patients with aneurysmal subarachnoid hemorrhage (SAH), and volume management is a critical component of its assessment. SAH is often associated with cardiopulmonary complications, including arrhythmia,1 cardiac dysfunction (neurogenic stunned myocardium),2-4 and neurogenic pulmonary edema,5-7 which also contribute to post-SAH morbidity and mortality. It is therefore important to develop reliable assessment modalities for close monitoring of systemic hemodynamic status after SAH. It has been reported that marked sympathetic activation is linked to cardiopulmonary complications,8,9 and studies have identified predictors of neurogenic manifestations based on chest

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x-ray, electrocardiogram, or cardiac ultrasound. However, little is known about cardiopulmonary complications based on systemic hemodynamic parameters after SAH.13-16 Because transpulmonary thermodilution (PiCCO; Pulsion Medical Systems, Munich, Germany) can measure important hemodynamic parameters without the need for cardiopulmonary catheterization,16,17 it has gained increasing acceptance in many intensive care units18,19 and for volume management in patients with SAH.13-16,20 Therefore, PiCCO monitoring may provide new insights into the characteristics of cardiopulmonary dysfunction after SAH and real-time hemodynamic status. This study aimed to determine whether location of the ruptured aneurysm has an impact on systemic cardiopulmonary hemodynamics after SAH and to assess the predictors of initial cardiopulmonary dysfunction after SAH based on hemodynamic parameters prospectively collected by the SAH PiCCO study group.

Methods Study Population Patients were included if they had a ruptured cerebral aneurysm diagnosed by cerebral angiography or 3dimensional angiography. The exclusion criteria were the following: (1) ,15 years of age; (2) absence of brainstem reflexes; (3) pregnancy; and (4) severe cardiopulmonary dysfunction requiring percutaneous cardiopulmonary support. Patients with rebleeding during the postoperative study period were also excluded because the accuracy of diagnosis of delayed cerebral ischemia (DCI) and the degree of pulmonary edema could be affected by rebleeding. The SAH PiCCO study was a multicenter prospective cohort study of SAH patients admitted to the 9 participating Japanese university hospitals. The study was approved by the appropriate ethics committees of all participating institutions, and written informed consent for treatment was obtained from all patients or their next of kin. The study was registered with the University Hospital Medical Information Network (UMIN) Clinical Trials Registry (http://apps.who.int/trialsearch/trial. aspx?trialid5JPRN-UMIN000003794): UMIN-CTR ID UMIN000003794. All patients admitted to the 9 participating institutions with aneurysmal SAH between October 2008 and March 2012 were screened for eligibility. Patients who were monitored using the PiCCO system during the perioperative period were included in the study. All patients underwent aneurysm treatment (clipping or coiling) within 48 hours of the onset of symptoms of SAH. Treatment decisions were at the discretion of the attending physician.

Single-indicator Transpulmonary Thermodilution (PiCCO) Monitoring All patients were monitored using PiCCO Plus on days 1-14 after SAH. A 4-French thermistor-tipped arterial catheter (PV2014L16; Pulsion Medical Systems, Munich, Germany) was inserted into the femoral or brachial artery. The arterial catheter and a central venous catheter were connected to pressure transducers and to the PiCCO Plus system for monitoring. Cardiac index (CI; normal range [NR], 3-5 L/minute/m2) and systemic vascular resistance index (SVRI; NR, 1700-2400 dyn/second/m2) were measured to assess afterload as left cardiac function and cardiac output. Global end-diastolic volume index (GEDI; NR, 680-800 mL/m2) was measured to assess preload as right cardiac function. Extravascular lung water index (EVLWI; NR, 3.0-10.0 mL/kg) and pulmonary vascular permeability index (PVPI; NR, 1.0-3.0) were also measured to assess pulmonary edema. Finally, global ejection fraction (GEF; NR, 25%-35%) was measured to assess cardiac contractility as a marker of cardiac failure. The parameters were determined by continuous cardiac output (CO) calibration by triplicate central venous injections of 15 mL of ice-cold saline (,8 C). CO was calculated by analysis of the thermodilution curve followed by pulse–contour analysis for continuous monitoring. Details of the PiCCO monitoring protocol have been described elsewhere.13,14

Postoperative Management Perioperative care was performed according to the standardized protocol for SAH provided by current American Heart Association guidelines.21 Postoperative B-type natriuretic peptide (BNP), a marker of cardiac failure, was measured on day 1 (acute phase) and days 12-14 (delayed phase), and laboratory testing of the blood was performed until day 14. Cardiopulmonary function was monitored throughout the analysis until day 14. Intracranial and cerebrospinal fluid pressure were controlled by ventricular, cisternal, or spinal drainage. Blood transfusion was performed when hemoglobin and hematocrit levels were below the lower limit of the normal range. Triple-H (hypervolemia, hypertension, and hemodilution) therapy was administered for symptomatic vasospasm at the discretion of the attending physician.

Statistical Analysis Data are presented as median values with 95% confidence intervals. Data were tested for normality of distribution and equal standard deviations using GraphPad InStat Version 3.10 (GraphPad Software, La Jolla, CA) to determine whether parametric or nonparametric assumptions should be used for each statistical method. Comparisons between groups were performed using the Mann–Whitney test for continuous variables and the c2 test for categorical

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range throughout the study period and was not significantly different among 4 groups (data not shown).

variables. Multivariate logistic regression analysis was performed to identify factors associated with poor cardiac contractility (GEF,25%) as a marker of cardiac failure in the postoperative 5 days (day 1-5) using SPSS (Version 15.0; SPSS Japan Inc, Tokyo, Japan). Unless stated otherwise, differences were considered statistically significant at P , .05.

Characteristics of CO and Afterload as Left Cardiac Function Cardiac output was evaluated using CI (Fig 1). There were specific findings that depended on the location of the ruptured aneurysm. In the acute phase, ICA aneurysm was associated with significantly lower CI compared with others on days 1 (P 5 .03) and 2 (P 5 .03). In the spasm phase, ACA aneurysm was associated with significantly lower CI on days 9 (P 5 .048), 10 (P 5 .03), 11 (P 5 .03), 12 (P 5 .003), and 13 (P 5 .03) compared with others, and VA/BA aneurysm was associated with significantly higher CI on days 8 (P 5 .02), 9 (P 5 .009), 10 (P 5 .03), and 11 (P 5 .005) compared with others. There were also some specific findings for SVRI (Fig 2). ACA aneurysm was associated with significantly lower SVRI on days 1 (P 5 .04) and 2 (P 5 .04) in the acute phase and with significantly higher SVRI on days 9 (P 5 .04), 10 (P 5 .04), 11 (P 5 .02), 12 (P 5 .003), 13 (P 5 .006), and 14 (P 5 .01); indicating afterload mismatch in the spasm phase. On the other hand, SVRI

Results Patient Characteristics Of 204 subjects enrolled, 58 had aneurysms of the anterior communicating artery (ACA), 61 of the middle cerebral artery (MCA), 57 of the internal carotid artery (ICA), and 28 of the vertebrobasilar artery (VA/BA). There were no significant differences in age, World Federation of Neurological Surgeons grade, Fisher group, aneurysm size, rebleeding rate, transfusion rate, triple-H therapy rate, x-ray–based pulmonary edema, DCI, or Glasgow Outcome Scale among the groups, except for predominance of coiling in VA/BA (P , .001, Table 1). The daily fluid intake and output were gradually increased in both groups until day 6 and then maintained at about 3000 to 4000 mL per day. Sodium balance was within the normal

Table 1. Clinical characteristics of patients Characteristics

ACA

MCA

ICA

VA/BA

N (male) Age WFNS grade I II III IV V Fisher group 1 2 3 4 Aneurysm size Clipping: coiling Rebleeding Transfusion Triple-H therapy X-ray–based pulmonary edema DCI GOS GR MD SD VS D

58 (26) 62.5 6 1.6

61 (20) 65.0 6 1.6

57 (10) 63.7 6 1.8

28 (9) 59.6 6 2.4

5 7 4 17 25

4 11 3 16 27

8 12 4 8 25

1 5 1 8 13

0 4 32 22 6.0 6 0.5 47:11 4 33 23 13 13

0 3 31 27 7.1 6 0.9 61:0 1 40 19 8 10

1 4 36 16 6.4 6 0.4 47:10 3 37 22 14 11

0 0 20 8 7.9 6 1.5 7:21 1 9 7 5 3

12 19 16 4 7

14 13 22 11 1

15 13 15 12 2

5 6 7 7 2

P value n.s n.s

n.s

n.s ,.001 n.s n.s n.s n.s n.s n.s

Abbreviations: ACA, anterior communicating artery; D, death; DCI, delayed cerebral ischemia; GOS, Glasgow Outcome Scale; GR, good recovery; ICA, internal carotid artery; MCA, middle cerebral artery; MD, moderate disability; SD, severe disability; VA/BA, vertebrobasilar artery; VS, vegetative state; WFNS, World Federation of Neurological Surgeons. n.s: not significant.

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Figure 1. Time course of changes in CI for 14 days after SAH. Abbreviations: ACA, anterior communicating artery; CI, cardiac index; ICA, internal carotid artery; MCA, middle cerebral artery; SAH, subarachnoid hemorrhage; VA/BA, vertebrobasilar artery. *P , .05, **P , .01, Mann–Whitney test.

after VA/BA aneurysm rupture was significantly lower on days 9 (P 5.03), 11 (P 5.03), and 13 (P 5.02); indicating a warm shock-like condition with hyperdynamic state in the spasm phase. It is also noteworthy that no specific characteristics of CI and SVRI were observed for MCA aneurysm compared with others. Postoperative BNP concentration and its temporal change were also evaluated with respect to aneurysm location (Fig 3). A significant decrease in BNP from acute to delayed phase (P 5 .02) was observed only with MCA aneurysm.

Characteristics of Pulmonary Edema and Preload as Right Cardiac Function Pulmonary edema was evaluated using EVLWI (Fig 4) and PVPI. Overall, EVLWI was around the upper limit of

the normal range, and PVPI (data not shown) was within the normal range throughout the study period, with a wide distribution. However, observed biphasic elevation of EVLWI was dependent on aneurysm location. EVLWI was significantly higher with ACA (day 1, P 5 .03) and MCA (day 2, P 5 .03) aneurysms in the acute phase and with ICA aneurysm (day 10, P 5 .04 and 12, P 5 .04) in the spasm phase, with no difference in PVPI. Preload was assessed with GEDI as right cardiac function. GEDI was above the upper limit of the normal range in all groups, with no specific differences with location (data not shown).

Predictors of Poor Cardiac Contractility as Cardiac Failure after SAH Finally, we assessed the predictors of poor cardiac contractility (GEF,25%) as a marker of cardiac failure

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Figure 2. Time course of changes in SVRI for 14 days after SAH. Abbreviations: ACA, anterior communicating artery; ICA, internal carotid artery; MCA, middle cerebral artery; SAH, subarachnoid hemorrhage; SVRI, systemic vascular resistance index; VA/BA, vertebrobasilar artery aneurysm. *P , .05, **P , .01, Mann–Whitney test.

in the postoperative 5 days (days 1-5) after SAH. Multivariate logistic regression analysis showed that age more than 65 years (odds ratio [OR], 4.62; 95% confidence interval, 1.93-11.06; P ,.001), Fisher group 4 (OR, .35; 95% confidence interval, .15-.82; P 5 .015), and ACA location (OR, 3.03; 95% confidence interval, 1.02-9.01; P 5 .046) were independent factors related to performance of heart muscle in the acute stage (Table 2).

Discussion Figure 3. Postoperative BNP values on day 1 (acute phase) and days 12-14 (delayed phase) for ACA, MCA, ICA, and VA/BA aneurysm locations. Abbreviations: ACA, anterior communicating artery; BNP, B-type natriuretic peptide; ICA, internal carotid artery; MCA, middle cerebral artery; VA/ BA, vertebrobasilar artery. *P , .05, Mann–Whitney test.

This study evaluates differences in cardiopulmonary hemodynamics with respect to the location of the ruptured aneurysm after SAH. Our data suggest that aneurysm location has an impact on left cardiac function but not on right cardiac function until day 14 after SAH.

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Figure 4. Time course of changes in extravascular lung water index (EVLWI) for 14 days after SAH. Abbreviations: ACA, anterior communicating artery; ICA, internal carotid artery; MCA, middle cerebral artery; SAH, subarachnoid hemorrhage; VA/BA, vertebrobasilar artery. *P , .05, Mann–Whitney test.

First, in the early phase, ICA aneurysm was associated with impaired left cardiac function. In the spasm period, ACA aneurysm was associated with afterload mismatch and VA/BA aneurysm with warm shock-like condition. MCA aneurysm had less impact on left cardiac function compared with others and was accompanied by improvement in BNP. Second, pulmonary edema was biphasic depending on aneurysm location, associated with ACA and MCA aneurysms in the acute phase and ICA aneurysm in the spasm phase independent from left cardiac dysfunction. Finally, patient age and ACA location were independent risks related to cardiac failure after SAH. SAH is associated with many unique, often inter-related systemic complications for respiratory,5-7 cardiac,2-4 endocrine,22 and hematopoietic systems23 outside the brain. It has been reported, based on autopsy findings

that systemic complications after SAH are related to hypothalamic damage,24,25 although the definitive mechanism has yet to be determined. Cardiac dysfunction is a wellrecognized SAH-related phenomenon, and myocardial abnormalities such as cardiac arrhythmias, electrocardiographic changes, and neurogenic stunned myocardium have been reported to occur within the first 5 days of SAH.4 Excess catecholamine release from sympathetic and adrenal medullary activation following hypothalamic damage has been proposed as an explanation for the development of myocardial irregularities,8,9 although whether the location of the ruptured aneurysm can affect cardiac dysfunction has not been clarified. In this study, location in the ACA resulted in lower vascular resistance in the acute phase and afterload mismatch in the spasm period, and multivariate analysis

ANEURYSM LOCATION AND SYSTEMIC HEMODYNAMICS IN SAH

Table 2. Odds Ratios for risk factors for cardiac contractility (GEF ,25%) in the acute phase after SAH Variable

95% CI

P value

1 4.62

reference 1.93-11.06

,.001

1 2.1

reference .89-4.98

.092

1 .35

reference .15-.82

.015

1 3.03 1.23 .68

reference 1.02-9.01 .42-3.6 .15-3.09

.046 .709 .616

1 .69

reference .19-2.46

.564

1 0.5

reference .2-1.25

.138

Adjusted OR

Age, y &64 65& WFNS grade I, II, III, IV V Fisher group 1, 2, 3 4 Aneurysm location ICA ACA MCA VA/BA Treatment Clipping Coiling Transfusion No Yes

Abbreviations: CI, confidence interval; ACA, anterior communicating artery; ICA, internal carotid artery; GEF, global ejection fraction; MCA, middle cerebral artery; OR, odds ratio; SAH, subarachnoid hemorrhage; VA/BA, vertebrobasilar artery aneurysm; WFNS, World Federation of Neurological Surgeons.

showed that ACA location was independently related to cardiac failure after SAH. These results support the hypothalamic damage theory of cardiac dysfunction following direct injury or perforator injury to hypothalamus due to ACA aneurysm rupture.26 Interestingly, the relationship between electrocardiographic abnormalities and location of intracranial aneurysms after SAH has been investigated previously, and results suggested that sinus bradycardia, prolonged QTc interval, inverted T waves, and presence of U waves were most prevalent with ACA aneurysm.1 Another article also reported high plasma BNP concentration in patients with ruptured ACA caused by direct mechanical damage at the anterior hypothalamus,27 although our study did not show significantly high BNP with ACA aneurysm on day 1 after SAH, possibly because of the difference in timing of BNP assessment. Based on postoperative hemodynamic assessment with PiCCO, our study confirms the hypothesis that a ruptured ACA affects cardiac dysfunction because of hypothalamic damage, and we have provided evidence that a ruptured MCA has less impact on cardiac dysfunction, and temporal improvement of BNP, after SAH. Interestingly, a warm shock-like condition was observed in the spasm period after VA/BA aneurysm. Most patients with VA/BA aneurysm underwent endovascular coil embolization, and postoperative C-reactive protein was significantly lower on day 3 and significantly

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higher during the spasm period (Fig 5). Postoperative inflammatory response from coils might contribute to this hemodynamic status in VA/BA aneurysm, but a lack of supporting data makes it is difficult to establish the mechanism. Previous reports have shown that postoperative perianeurysmal edema could be because of an inflammatory response from coils,28,29 and further assessment of this phenomenon is necessary. Pulmonary complications, including neurogenic pulmonary edema, are also potentially life-threatening complications in patients with SAH.5-7 Neurogenic pulmonary edema is a clinical syndrome characterized by the acute onset of pulmonary edema following a significant central nervous system insult such as SAH, spinal cord injury, traumatic brain injury, or intracranial hemorrhage.30 Neurogenic pulmonary edema is also thought to be caused by a catecholamine surge that results in cardiopulmonary dysfunction,31 and several mechanisms have been proposed: (1) neurocardiac,32 (2) neurohemodynamic,33 (3) blast theory,34 and (4) pulmonary venule adrenergic hypersensitivity.35 Friedman et al14 found pulmonary complications in 22% of patients with SAH, including neurogenic pulmonary edema in 2%, nosocomial pneumonia in 9%, congestive heart failure in 8%, and aspiration pneumonia in 6%. However, it is still difficult to evaluate neurogenic pulmonary edema with chest x-ray findings and clinical symptoms, which have lower sensitivity and specificity because of the lack of hemodynamic assessment.36-38 Our study shows that extravascular lung water was high and biphasic depending on aneurysm location (ACA and MCA in the acute phase and ICA in the spasm phase) but permeability was not affected. Consequently, clinical grade and amount of subarachnoid blood has to be taken into account to estimate the probability of the occurrence of neurogenic pulmonary edema, as previously discussed.7 It has also been reported that the incidence of neurogenic pulmonary edema was significantly higher in patients with ruptured aneurysm in the posterior circulation, as assessed from chest x-ray or clinical symptoms.7 Based on the quantitative hemodynamic assessment in this study, EVLWI with VA/BA aneurysm was similar to that in other locations. It has recently been reported that there is no link between neurogenic pulmonary edema and VA/BA localization,6, which supports our results, and that increased intracranial pressure during the acute phase is a risk factor for developing neurogenic pulmonary edema.6 That study also mentioned that neurogenic pulmonary edema might occur independent of hemodynamic mechanisms6 because several studies have postulated that adrenergic receptors modulate endothelial permeability in pulmonary microvessels directly.5 Our results also showed that location-specific left cardiac dysfunction did not affect extravascular lung water, supporting pulmonary venule adrenergic hypersensitivity as the mechanism of neurogenic pulmonary edema.35

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Figure 5. Time course of changes in C-reactive protein for 14 days after SAH. Abbreviations: ACA, anterior communicating artery; CRP, C-reactive protein; ICA, internal carotid artery; MCA, middle cerebral artery; SAH, subarachnoid hemorrhage; VA/BA, vertebrobasilar artery. *P , .05, **P , .01, Mann–Whitney test.

Regarding the treatment strategy for DCI after SAH, we have previously shown that low CI and high SVRI as well as low GEDI were independent factors related to onset of DCI after SAH.14 The findings of this study provide important insights into a strategy for volume management. For ACA aneurysm demonstrating afterload mismatch (low CI and high SVRI) in the spasm phase, decreasing fluid administration (lowering GEDI) for cardiac failure should be avoided so as not to facilitate DCI. Rather, SVRI should be lowered with antihypertensive agents. Where VA/BA aneurysm results in warm shock-like condition (high CI and low SVRI) in the spasm phase, increased fluid administration should be avoided because GEDI is already very high. Alternatively, increasing blood pressure is necessary to improve peripheral circulatory failure.

Several limitations of this multicenter cohort study should be discussed. First, we did not evaluate catecholamine levels because they were not available. Second, cardiac function was evaluated using PiCCO data, and data from conventional echocardiography or electrocardiography evaluations were not obtained. Nevertheless, bedside monitoring using PiCCO is a powerful, established tool for the assessment of cardiopulmonary hemodynamics,13-16,18-20 and we believe postoperative hemodynamic assessment is critical to the management of cardiopulmonary conditions and vasospasm in SAH.

Conclusions Aneurysm location drastically affects left cardiac function but not right cardiac function until day 14 after SAH.

ANEURYSM LOCATION AND SYSTEMIC HEMODYNAMICS IN SAH

Location in the MCA has less impact than other locations on left cardiac function. Pulmonary edema is biphasic depending on the aneurysm location, but not always parallel to cardiac dysfunction. Age and ACA location may be risk factors for cardiac failure after SAH. Acknowledgment: SAH PiCCO Study Group: Department of Emergency and Critical Care Medicine, Nippon Medical School Hospital; Department of Neurosurgery, Kansai Medical University Hirakata Hospital; Department of Neurosurgery, Tokyo Medical and Dental University, University Hospital of Medicine; Department of Neurosurgery, Fukuoka University Hospital; Department of Neurosurgery, Nagasaki University Hospital; Department of Neurosurgery and Clinical Neuroscience, Yamaguchi University School of Medicine; Department of Emergency and Critical Care Medicine, Nippon Medical School Tama Nagayama Hospital; Department of Neurosurgery, Saitama Medical University General Medical Center; Department of Neurosurgery, Saitama Medical University International Medical Center.

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Impact of aneurysm location on cardiopulmonary dysfunction after subarachnoid hemorrhage.

Cardiopulmonary dysfunction may occur after aneurysmal subarachnoid hemorrhage (SAH), but its characteristics have not been fully clarified. We invest...
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